Journal of Biological Control, 26 (4): 297–313, 2012
Review Article
The ladybird predator Serangium parcesetosum Sicard (Coleoptera: Coccinellidae): current
status and future perspectives
FIRAS AL-ZYOUD
Department of Plant Protection and IPM, Faculty of Agriculture, Mu'tah University, Karak, 61710, Jordan
Corresponding author E-mail: firaszud@yahoo.com
ABSTRACT: Whiteflies have been causing extensive damage for almost a century and continue to be destructive pests of several
agricultural crops in much of the world. Biological control is recognized as the best alternative to the use of insecticides for controlling
insect pests. Serangium parcesetosum Sicard (Col., Coccinellidae) is a specialist, oligophagous and efficient predator that has demonstrated
a potential for biological control of many whitefly species. Concomitantly, this paper reviews the morphology, phenology and biology
of S. parcesetosum. In addition, studies conducted during the last decade on the predator’s predation potential and preferences are
summarized. Furthermore, S. parcesetosum releases against some whitefly species are herein presented. Finally, this paper presents the
current efforts in biological control of whiteflies using S. parcesetosum in greenhouses and open fields, and highlights research gaps
and directions deserving further development to create a better understanding of S. parcesetosum on different agricultural crops to
control whiteflies. The available data indicate that long survival of S. parcesetosum adults accomplished by their voracious feeding is
a great feature that resulted in successful control of whiteflies. An additional positive feature of S. parcesetosum is that it could establish
and disperse throughout citrus fields. In conclusion, S. parcesetosum could develop, survive, reproduce and prey upon whiteflies, and
build up its population successfully. Consequently, it is likely that S. parcesetosum could effectively function as a sole biological control
agent or in conjunction with other natural enemies to develop new management strategies to provide a great level of suppression of
whiteflies worldwide.
KEY WORDS: Serangium parcesetosum, predator, whiteflies, biology, predation, preference, population dynamics, biological
control
(Article chronicle: Received: 03-08-2012;
Revised: 02-11-2012;
INTRODUCTION
Accepted: 14-12-2012)
of biological pest control by coccinellids (Majerus, 1994).
About 6000 species of Coccinellidae are known Worldwide
(Vandenberg, 2000) with over 300 species known from
the Indo-Pakistan subcontinent (Rahatullah et al., 2010).
Poorani (2002) has given an annotated checklist of the
family Coccinellidae for the Indian sub-region, which
lists 400 species, under 79 genera, 22 tribes and five
subfamilies. Thirty one species were identified, of which
19 species were recorded for the first time within the
Haridwar district of India (Joshi and Sharma, 2008).
Fourteen species from 12 genera belonging to 4 subfamilies
were listed in Pakistan (Rahatullah et al., 2011). Also,
Khan et al. (2007) have recorded 12 species of coccinellid
beetles from Chitral district of Pakistan. Shah (1985)
studied the coccinellids of Peshawar valley and recorded
16 species along with geographical distribution and
host plants. Singh and Singh (1990) have reported
16 species of aphidophagous coccinellids from Mizoram
state, a north eastern state of India. In addition, Omkar
and Pervez (2000, 2002) have reported 17 more species
Coccinellidae (Coleoptera) is a wellknown beetle
family, worldwide distributed (Almeida et al., 2011), and
divided into six subfamilies: Coccidulinae, Coccinellinae,
Scymninae, Chilocorinae, Sticholotidinae and Epilachninae
(Vandenberg, 2002). The predaceous insects of family
Coccinellidae are commonly known variously as ladybirds,
ladybugs, lady beetles or coccinellid beetles (Sharma and
Joshi, 2010). Predaceous ladybird beetles occur within
the first five subfamilies whereas the Epilachninae are
phytophagous (Hodek and Honek, 1996; Dixon, 2000).
The coccinellids are of extremely diverse habits, predators
of a variety of pests such as aphids, leafhoppers, scale
insects, mealybugs, whiteflies, thrips and mites in all parts
of the world (Majerus, 1994; Omkar and Bind, 1996;
Al-Zyoud, 2007, 2008, 2012). The introduction of the
Vedalia ladybird, Rodolia cardinalis Mulsant from
Australia into California in 1888 to control the cottony
cushion scale, Icerya purchasi, which threatened the citrus
industry, is widely regarded as the most successful instance
297
FIRAS AL-ZYOUD
controversial. The green lacewing, Chrysoperla carnea
(Stephens) (Abd-Rabou and El-Naggar, 2003), and the
phytoseiid predatory mites, Euseius scutalis (AthiasHenriot) and Typhlodromips swirskii (Athias-Henriot)
appear to be promising biological control agents of
whiteflies (Nomikou et al., 2003). Many species of
Coccinellidae are considered important natural enemies
of whiteflies and may exhibit various degrees of oligophagy
(Obrycki and Kring, 1998). Delphastus catalinae (Horn)
feeds on immature whitefly but there are conflicting
reports on prey consumption rates (Heinz and Parrella,
1994a).
of coccinellids from the same region. Also, in India,
8 species of ladybird beetles belonging to 6 genera were
recorded (Sharma et al., 2011). Similarly, Usman and
Puttarudriah (1955) recorded 48 species of predaceous
coccinellids from the Mysore state, to which Kapur
(1972) further added 17 species. Furthermore, 30 coccinellid
species belonging to 18 genera (Pajni and Singh,
1982) and 25 coccinellid species from 15 genera from
the Chandigarh region (Pajni and Varma, 1985) were
recorded.
Biological control of whiteflies through the release
of natural enemies has been attempted for at least 30
years (Goolsby et al., 2000), and many attempts have
ended in complete success. Some species of fungi
such as Aschersonia aleyrodis, Verticillium lecanii,
Paecilomyces fumosoroseus and Beauveria bassiana
have been developed as microbial agents against whiteflies
(Mor et al., 1996; Chen and Feng, 1999; James and
Jaronski, 2000), but, the development of fungi as control
agents of whiteflies is still at a fairly early stage. However,
extensive listed fauna of parasitoids were used to
control whiteflies of various species of the genera
Eretmocerus and Encarsia (DeBarro et al., 2000;
Hu et al., 2003; Urbaneja and Stansly, 2004). Nevertheless,
the required releases of Er. eremicus (Rose and Zolnerowich)
were 27-fold more expensive than the use of insecticides
(Driesche et al., 1999). Moreover, En. formosa Gahan
was unable to build-up its populations on B. tabaci and
its activity is reduced during winter (Arno and Gabarra,
1996). Nevertheless, in spite of whiteflies being hosts of
many parasitoids, it seems that the control of these pests
by parasitoids is not achieved due to the extensive host
range and mobility of the pests (Gerling and Steinberg,
2003). Thus, biological control strategies should include
the release of additional natural enemies.
The genus Serangium (Coleoptera: Coccinellidae) was
erected by Blackburn (1889) with Serangium mysticum
Blackburn from Australia as the type species. The name
Serangiini was introduced by Blackwelder (1945) in his
checklist and was validated by Pope (1962). Serangium
is the largest genus of Serangiini with 45 described
species, mostly occurring in the Oriental Region (Slipinski
and Burckhardt, 2006). Wang et al. (2011) reviewed and
described 12 species of Serangium from China. Serangium
spp. are widely distributed in the World and known to
be useful predators of many whitefly species. Serangium
parcesetosum Sicard is a specialist, oligophagous and
efficient predator that has demonstrated a potential for
the biological control of many whitefly species.
S. parcesetosum was firstly found in India and described
by Sicard (1929) and reported there to be a very host
specific on the cotton whitefly, Bemisia tabaci (Genn.)
(Kapadia and Puri, 1992) and on the sugarcane whitefly,
Aleurolobus barodensis Mask. (Shah et al., 1986; Patel
et al., 1996). This predatory species was originally
collected from India in 1929 for the release as a bioagent of the citrus whitefly, Dialeurodes citri (Ashmead)
in the Union of Soviet Socialist Republic (Timofeyeva
and Nhuan, 1979). According to field studies carried out
in Turkey, S. parcesetosum has successfully adapted in
citrus growing areas to control D. citri (Ulusoy et al.,
1996). S. parcesetosum was introduced into Georgia in
1974 and into France from Georgia in 1985 for the
biological control of D. citri (Malausa et al., 1988). This
ladybird was released to control the wooly whitefly,
Aleurothrixus floccosus Maskell in Israel (Argov, 1994),
and B. tabaci and D. citri in Syria (Abboud and
Ahmad, 1998 Ahmad and Abboud, 2001). In addition,
S. parcesetosum was investigated as a predator of the
silverleaf whitefly, Bemisia argentifolii Bellows and
Perring (B. tabaci biotype B) in the USA (Ellis et al.,
2001; Legaspi et al., 2001). S. parcesetosum release was
evaluated in grapefruit orchard to control the citrus
blackfly, Aleurocanthus woglumi Ashby (Legaspi et al.,
2001). The biological and ecological parameters of
Predators play a key role in regulating pest populations
(Jazzar and Hammad, 2004). Predators range from
generalists that require additional food and specialists
whose metabolism is adjusted to a specific biochemical
composition of food. Hundreds of predators have been
reported to prey upon whiteflies including arthropods
belonging to 9 orders and 31 families. Heteropteran
predators are usually polyphagous and prey specificity is
rare (Fauvel, 1999). The predatory mirid bug, Dicyphus
tamaninii Wagner (Lucas and Alomar, 2002) and
Nesidiocoris tenuis Reuter (Calvo et al., 2009), and
the anthocorid bugs, Orius laevigatus (Fieber) and
O. majusculus (Reuter) (Montserrat et al., 2000) were
used to control whiteflies. However, plant feeding by some
species of predatory Heteroptera may cause economic
injury (Sanchez and Lacasa, 2008) making their use
298
Serangium parcesetosum: current status and future perspectives
in large groups. S. parcesetosum emerges from its winter
hibernation at early April. Thereafter, S. parcesetosum feeds
actively for 40–50 days on its prey eggs and larvae, after
which it started egg laying, and continues to lay eggs until
end of June. S. parcesetosum has 4–5 generations/year
(Timofeyeva and Nhuan, 1979). The predator lays its
eggs singly or in groups on the under surface of the leaf
among the whitefly eggs (Ahmad and Abboud, 2001;
Al-Zyoud et al., 2005b). The first larval instar (L1) to
hatch frequently consumes the eggs on their own egg
batch. Newly hatched L1 are relatively immobile and feed
on whitefly eggs and larvae over a limited leaf surface.
The L2 and L3 move rapidly over the leaves, like the
adults, they feed on all development stages of the host
(Patel et al., 1996; Ellis et al., 2001; Al-Zyoud and
Sengonca, 2004). Males of S. parcesetosum follow females,
feeding on the remains of the prey of the females and
rarely feeding independently. Having attached themselves,
pupae frequently become the victims of cannibalism by
older larvae (Timofeyeva and Nhuan, 1979).
S. parcesetosum have thoroughly been investigated on
B. tabaci (Al-Zyoud and Sengonca, 2004; Al-Zyoud
et al., 2004, 2005b, 2006; Sengonca et al., 2004, 2005;
Al-Zyoud, 2007, 2008). According to Al-Zyoud et al.
(2005a), S. parcesetosum was found to be a promising
predator of the greenhouse whitefly, Trialeurodes
vaporariorum Westwood. S. parcesetosum releases were
evaluated to control B. tabaci on cotton and cucumber
(Al-Zyoud et al., 2007; Al-Zyoud, 2012), and B. argentifolii
on poinsettias (Ellis et al., 2001) under greenhouse
conditions.
Concomitantly, this paper reviews the morphology,
phenology and biology of S. parcesetosum. In addition,
the studies conducted during the last decades on the
predator’s predation potential and preferences are
summarized. Finally, S. parcesetosum releases against
some whitefly species are herein presented. Also, this
paper presents the current efforts in biological control of
some whiteflies using S. parcesetosum in greenhouses
and open fields, and highlights research gaps and
directions deserving further development to create a
better understanding of this predator on different
agricultural crops to control whiteflies.
Prey species of Serangium parcesetosum
The predator, S. parcesetosum feeds successfully upon
many whiteflies in the family Aleyrodidae (Hom.), including
B. tabaci (Al-Zyoud et al., 2006, 2007; Al-Zyoud, 2008),
A. barodensis (Kapadia and Butani, 1997; Patel et al.,
1996), D. citri (Yigit, 1992b; Uygun et al., 1997; Yigit
et al., 2003), B. argentifolii (Ellis et al., 2001; Legaspi
et al., 2001), A. floccosus (Argov, 1994), T. vaporariorum
(Al-Zyoud et al., 2005a), A. woglumi (Kalidas, 1995),
the castor bean whitefly, Trialeurodes ricini (Misra)
(Al-Zyoud, 2007), the spiraling whitefly, Aleurodicus
dispersus (Russell) and the arecanut whitefly, Aleurocanthus
arecae David (Legaspi et al., 1996). From the family
Coccidae (Homoptera), S. parcesetosum has been reported
to feed on the brown soft scale, Coccus hesperidum
L. (Yigit et al., 2003), the citrus soft scale, C. pseudomagnoliarum (Kuwana) (Abboud et al., 2009), and the
striped mealybug, Ferrisia virgata (Cockerell) (Legaspi
et al., 1996).
MORPHOLOGY AND PHENOLOGY OF SERANGIUM
PARCESETOSUM
The adult of S. parcesetosum is small, hemispherical,
shiny, and yellow-brown. The fronts’ mouthparts and legs
are usually slightly lighter, and the eyes are black. The
head is sub-merged into pronotum, and directed downward.
Antennae have 9 segments, where the 4th-8th segments
are equal. Legs are covered with hairs and the femur
strongly broadened and tarsi conceitedly 4 segmented.
The abdomen is semicircular. Adult’s body length is
2.0–2.1 mm, width of 1.7–1.8 mm and depth of 1.1 mm
(Timofeyeva and Nhuan, 1979; Poorani, 1999). The last
larval instar is 4.0–5.3 mm in length, fusiform in shape,
and widest on the metathorax. Larval head has indistinct
brownish spots, and has 3 black ocelli on each side,
and the antenna is short with 3 segments. The larval
1st – 8th abdominal segments are almost of identical length,
following segments gradually narrowing to the end. Larval
body is densely covered with setae surrounded by
pigmented areas, and legs are long and slender with
sparse hairs, and brown claw. The pupa is 2.3–2.4 mm
long, 1.8 mm wide, white yellowish, covered with dense
long gray hairs on prothoracic segment (Timofeyeva and
Nhuan, 1979).
Biology of Serangium parcesetosum
In order to use a predator in biological control
programs against a pest species, it is important to
investigate its biology, which is considered one of the
most important features that should be taken into
account. However, the biology of S. parcesetosum has
been affected by temperature, prey’s host plant species or
cultivar, and prey species or even strain (Abboud and
Ahmad, 1998, 2006; Al-Zyoud et al., 2004, 2005a, b;
Al-Zyoud, 2008). Summarizing the data available on
The predator, S. parcesetosum overwinters as adult
in dry rolled up leaves and underneath bark, congregating
299
FIRAS AL-ZYOUD
biology of S. parcesetosum may enhance the options for
using this specialized predator in pest management
programs to control whiteflies in both greenhouses and
open fields.
have four larval instars during development. However,
prey species, temperature, prey’s host plant species and
predatory sex influence the developmental duration of
S. parcesetosum as shown in Table 1. Data indicate that
males develop faster than females do in all studies
undertaken (Sengonca et al., 2004; Al-Zyoud et al.,
2005a; Al-Zyoud, 2008). At the same temperature and
prey species, S. parcesetosum develops faster on cotton
than cucumber (Sengonca et al., 2004), and on cabbage
than eggplant. This indicates that plant species plays
a key role in the development of the predator. The
shortest developmental duration (13.2 days) was recorded
when the predator reared at 27°C on sugarcane infested
with A. barodensis (Patel et al., 1996), while the longest
development was reported at 18°C on cucumber infested
with B. tabaci (45.2 days). Besides, this also indicates
that temperature plays a vital role in the development
of S. parcesetosum since the developmental duration is
3-fold at 18°C than at 27°C.
Development
The predator, S. parcesetosum is able to complete its
development on many whitefly species i.e. B. tabaci
(Al-Zyoud, 2008), A. barodensis (Patel et al., 1996),
D. citri (Yigit et al., 2003), B. argentifolii (Ellis et al.,
2001), A. floccosus (Argov, 1994), T. vaporariorum
(Al-Zyoud et al., 2005a), A. woglumi (Legaspi et al.,
2001), T. ricini (Al-Zyoud, 2007), A. dispersus and
A. arecae (Legaspi et al., 1996). The development of
S. parcesetosum consists of an egg stage, four larval
instars and a pupal stage (Patel et al., 1996; Abboud and
Ahmad, 1998; Sengonca et al., 2004; Al-Zyoud et al.,
2005a; Al-Zyoud, 2008). Klausnitzer and Klausnitzer
(1997) mentioned that most of the well-known coccinellids
Table 1. Mean developmental duration from egg to adult emergence of Serangium parcesetosum fed on different whitefly
species reared on different plants and temperatures
Temp
(°C)
Prey species
Plant species
Predator Sex
Developmental
duration (days)
Reference
18
Bemisia tabaci
Cotton
Male
43.4
Sengoncaet al. (2004)
18
B. tabaci
Cotton
Female
42.4
Sengonca et al. (2004)
18
B. tabaci
Cucumber
Male
45.2
Sengonca et al. (2004)
18
B. tabaci
Cucumber
Female
43.4
Sengonca et al. (2004)
21
B. tabaci
Cabbage
–
23.8
Ahmad and Abboud (2001)
25
B. tabaci
Cabbage
–
15.8
Abboud and Ahmad (1998)
25
Aleurothrixus floccosus
Cabbage
–
17.3
Abboud and Ahmad (1998)
25
Dialeurodes citri
Cabbage
–
17.9
Abboud and Ahmad (1998)
25
Bemisia tabaci
Cucumber
Male
20.0
Al-Zyoud (2008)
25
B. tabaci
Cassava
–
21.0
Asiimwe et al. (2007)
25
B. tabaci
Cotton
–
22.9
Vatanesever et al. (2003)
25
B. tabaci
Egg plant
–
28.0
Vatanesever et al. (2003)
23–33
B. tabaci
Cucumber
Male
17.4
Al-Zyoud (2008)
27
Aleurolobus barodensis
Sugarcane
–
13.2
Patel et al. (1996)
27
Bemisia tabaci
Cabbage
–
15.7
Ahmad and Abboud (2001)
27–32
B. tabaci
Cabbage
–
12.9
Ahmad and Abboud (2001)
30
B. tabaci
Cotton
Male
17.2
Sengoncaet al. (2004)
30
B. tabaci
Cotton
Female
16.2
Sengonca et al. (2004)
30
B. tabaci
Cucumber
Male
15.9
Sengonca et al. (2004)
30
B. tabaci
Cucumber
Female
15.1
Sengonca et al. (2004)
30
Trialcurodes vaporariorum Cucumber
Male
17.4
Al-Zyoud et al. (2005a)
30
T. vaporariorum
Cucumber
Female
16.9
Al-Zyoud et al. (2005a)
32
Bemisia tabaci
Cabbage
–
14.3
Ahmad and Abboud (2001)
300
Serangium parcesetosum: current status and future perspectives
Mortality
B. tabaci (21%) (Sengonca et al., 2004) reared on
cucumber at 30°C. Furthermore, mortality might be
affected by the combination of plant-whitefly-predator
(tritrophic) interaction.
Mortality occurs during all developmental stages of
S. parcesetosum. Mortality in L1 instar was the highest
as compared to other larval instars, and the mortality
in the pupal stage was the highest compared to other
immature stages (Sengonca et al., 2004; Al-Zyoud et al.,
2005a; Al-Zyoud, 2008). Temperature influences the
mortality of S. parcesetosum, of which it was higher
at 18°C (33 and 31%) than at 30°C (24 and 21%) on
cotton and cucumber infested by B. tabaci, respectively
(Sengonca et al., 2004). Abboud and Ahmad (1998)
stated that mortality of S. parcesetosum fed on B. tabaci
was 40, 22, 20% and 10% at 32, 27, 21°C and 27-32°C,
respectively. In addition, plant species influenced the
predator’s mortality, that is, it was higher on cotton than
cucumber (Sengonca et al., 2004). According to Ahmad
and Abboud (2001), the mortality was 100, 30, 18% and
5%, when S. parcesetosum fed on B. tabaci on bean,
cabbage, eggplant and okra at 27°C, respectively. In
addition, mortality was the lowest on cotton (21%)
and the highest on eggplant (49%) at 25°C (Vatanesever
et al., 2003). It was suggested that hair density on
plant leaves helps positively in reducing the predator’s
mortality (Ahmad and Abboud, 2001; Sengonca et al.,
2004). Furthermore, mortality is affected by prey species,
given that it was higher when S. parcesetosum fed on
T. vaporariorum (26%) (Al-Zyoud et al., 2005a) than on
Sex ratio
Sex ratio (female : male) of S. parcesetosum fed
on B. tabaci is affected by temperature and plant species.
It was 1:0.9 and 1:0.8 at 18°C, and 1:1.1 at 30°C on
cotton and cucumber under laboratory conditions,
respectively (Sengonca et al., 2004). Kapadia and Puri
(1992) reported a sex ratio of 1:0.8 and 1:1 under field
and laboratory conditions, respectively.
Longevity
One of the most important features for a successful
predator is to survive for a long period and feed continuously
on the prey species. Long survival of S. parcesetosum
adults (Sengonca et al., 2004) accomplished by voracious
feeding (Sengonca et al., 2005) is a great feature that
results in a successful control of B. argentifolii (Ellis
et al., 2001) and B. tabaci (Sengonca et al., 2004;
Al-Zyoud, 2008). However, S. parcesetosum longevity
varies according to temperature, prey’s host plant species
or cultivars, prey species or even strains and predatory
sex as shown in Table 2. The longest longevity (6 months)
Table 2. Mean longevity of Serangium parcesetosum fed on different whitefly species reared on different plants
and temperatures
Temp
(°C)
Prey species
Plant species
Predator Sex
Longevity
period (days)
Reference
18
18
18
18
30
30
30
30
30
30
25
23–33
25
23–33
23.7
23.7
27
20–23
20–23
20–23
20–23
20
30
40
Bemisia tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
Trialcurodes vaporariorum
T. vaporariorum
Bemisia tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
B. tabaci
Aleurolobus barodensis
Bemisia argentifolii
B. argentifolii
B. argentifolii
B. argentifolii
B. argentifolii
B. argentifolii
B. argentifolii
Cotton
Cotton
Cucumber
Cucumber
Cotton
Cotton
Cucumber
Cucumber
Cucumber
Cucumber
Cucumber
Cucumber
Cucumber
Cucumber
Egg plant
Egg plant
Sugarcane
Hibiscus
Cucumber
Cantaloupe
Tomato
Cantaloupe
Cantaloupe
Cantaloupe
Male
Female
Male
Female
Male
Female
Male
Female
Male
Female
Male
Male
Female
Female
Male
Female
–
–
–
–
–
–
–
–
175.4
144.5
122.2
94.3
92.4
52.5
63.4
50.3
70.8
59.9
79.9
95.1
65.2
71.5
50.5
22.6
29.8
44.2
24.5
27.6
27.8
79.2
26.9
1.40
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Sengonca et al. (2004)
Al-Zyoud et al. (2005a)
Al-Zyoud et al. (2005a)
Al-Zyoud (2008)
Al-Zyoud (2008)
Al-Zyoud (2008)
Al-Zyoud (2008)
Kapadia and Puri (1992)
Kapadia and Puri (1992)
Patel et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
Legaspi et al. (1996)
301
FIRAS AL-ZYOUD
was reported on cotton infested by B. tabaci at 18°C
(Sengonca et al., 2004), while the shortest (1.4 days)
was recorded on cantaloupe infested by B. argentifolii
at 40°C (Legaspi et al., 1996). Moreover, within the
same temperature S. parcesetosum survives longer on
cotton than cucumber (Sengonca et al., 2004), and on
hibiscus than cucumber, cantaloupe and tomato (Legaspi
et al., 1996). In all studies, females survive longer than
males do. It is worth mentioning that the extremely
high longevity on cotton may partly be explained by that
S. parcesetosum was reared on B. tabaci using cotton
as a host plant. Therefore, it might be that the predator
has adapted itself on cotton plants and lived much
more on it (Legaspi et al., 1996; Al-Zyoud et al., 2004).
Additionally, the morphological characteristics of the
host plant and the interaction of the plant-whiteflypredator (tritrophic) may have a major effect on the
longevity of the predator, suggesting a high degree of
specialization of S. parcesetosum on a plant species.
S. parcesetosum lived longer when the predator fed
on T. vaporariorum than on B. tabaci (Al-Zyoud
et al., 2005a), B. argentifolii (Legaspi et al., 1996), and
A. barodensis (Patel et al., 1996).
these predatory insects. In case of S. parcesetosum, a
growth medium composed of a mixture of an adherent
and fibrous retention substrate, a protein-lipid paste, and
a liquid was successfully used to rear the predator for
three generations (Hodek and Honek, 2009). In addition,
it was found that S. parcesetosum adults survive on
honey emulsion for 27 days at 18°C, and for 14 days at
30°C (Al-Zyoud et al., 2006).
Fecundity
The ability of a predator to oviposit successfully on
the host plant on which its prey lives is one of the major
factors in determining its ability to successfully control
the pest. Prey’s host plant species or even cultivar
temperature and prey species influence the daily and
total fecundity of S. parcesetosum. The maximum number
of eggs laid per day by S. parcesetosum was 4.7 eggs/
female (fed on B. tabaci Sengonca et al., 2004) and 1.5
eggs/female (fed on T. vaporariorum Al-Zyoud et al.,
2005a) on cucumber at 30°C. A maximum daily laid eggs
of 8.7 and 6.6 eggs/female was reported when S.
parcesetosum fed on B. tabaci at 25°C and 23-33°C,
respectively (Al-Zyoud, 2008). The highest total fecundity
of S. parcesetosum (443.9 eggs/female) was recorded on
cabbage when the predator fed on B. tabaci at 27°C
(Ahmad and Abboud, 2001) as shown in Table 4. This
was followed by 354.7 eggs/female when the predator
fed on B. tabaci on cotton at 25°C (Vatanesever et al.,
2003). It seems that temperature ranges from 25°C to
27°C is the most preferred for the predator. Within the
same temperature and plant species, the fecundity is
3-fold higher when S. parcesetosum fed on B. tabaci
(98 eggs/female) (Sengonca et al., 2004) than on
T. vaporariorum (28 eggs/female) (Al-Zyoud et al., 2005a).
In addition, when S. parcesetosum kept together with
5 different plant species infested with B. tabaci, the
predator laid more eggs on cucumber (115 eggs) than on
tobacco (42 eggs), cotton (33 eggs), tomato (30 eggs),
The periods of pre-oviposition, oviposition and
post-oviposition are affected by temperature, prey and
plant species as shown in Table 3. Range of periods of
pre-oviposition, oviposition and post-oviposition were
6.8-26.3, 24.3-121.1 and 8.6-59.7 days, respectively.
The ability of a natural enemy to survive on alternative
nutritional sources may have an advantage in stabilizing
its population dynamics (Lalonde et al., 1999). However,
a major stumbling block to use biological control on a
large scale is that it has been difficult to produce adequate
numbers of predatory insects to effect reduction of large
outbreaks of pest populations. For example, predators
have been used successfully for decades to control insect
pests however, the scale of their use has been limited
because of inadequate methods to artificially produce
Table 3. Mean pre-oviposition, oviposition and post-oviposition periods of Serangium parcesetosum fed on different
whitefly species reared on different plants and temperatures
Temp (°C)
Prey species
Plant species
Pre-ovip.
Ovip.
Post-ovip
Reference
18
Bemisia tabaci
Cotton
18.8
121.1
35.5
Sengonca et al. (2004)
18
B. tabaci
Cucumber
26.3
36.2
59.7
Sengonca et al. (2004)
30
B. tabaci
Cotton
07.7
28.0
56.7
Al-Zyoud et al. (2004)
30
B. tabaci
Cucumber
12.1
40.6
10.7
Al-Zyoud et al. (2004
30
Trialcurodes vaporariorum
Cucumber
08.8
46.0
16.0
Al-Zyoud et al. (2005a)
23.7
Bemisia tabaci
Eggplant
16.3
24.3
08.6
Kapadia and Puri (1992)
23–33
B. tabaci
Cucumber
06.8
52.5
35.8
Al-Zyoud (2008)
25
B. tabaci
Cucumber
08.2
42.3
29.5
Al-Zyoud (2008)
302
Serangium parcesetosum: current status and future perspectives
Table 4. Mean total fecundity of Serangium parcesetosum fed on different whitefly species reared on different
plants and temperatures
Temp (°C)
Prey species
Plant species
Fecundity
Reference
18
Bemisia tabaci
Cotton
52
Sengonca et al. (2004)
18
B. tabaci
Cucumber
25
Sengonca et al. (2004)
30
B. tabaci
Cucumber
98
Sengonca et al. (2004)
30
B. tabaci
Cotton
31
Sengonca et al. (2004)
30
Trialeurodes vaporariorum
Cucumber
28
Al-Zyoud et al. (2005a)
25
Bemisia tabaci
Cucumber
228
Al-Zyoud (2008)
23–33
B. tabaci
Cucumber
143
Al-Zyoud (2008)
23.7
B. tabaci
Eggplant
22.7
Kapadia and Puri (1992)
27
B. tabaci
Cabbage
443.9
Ahmad and Abboud (2001)
20–23
Dialeurodes citri
Citrus
135–185
Timofeyeva and Nhuan (1979)
25
B. tabaci
Eggplant
135.2
Vatanesever et al. (2003)
25
B. tabaci
Cotton
354.7
Vatanesever et al. (2003)
and sweet pepper (only 3 eggs) (Al-Zyoud et al., 2004).
Host plant and prey species have a major impact on natural
enemies by influencing their searching success and the
quality of their dietary resources, and consequently their
biology (Coll and Ridgway, 1995). Several researchers
have stated that plant architecture and surface texture
influence the search behavior of coccinellid predators
(Kareiva and Sahakian, 1990). Sweet pepper has overly
smooth leaf surfaces which may have a negative effect on
the oviposition of the predator (Carter et al., 1984). The
other four plants are characterized by hairiness leaf
surfaces therefore, it might be that leaf pubescence helps
positively increase the probability of more eggs being laid
enhacing the protection of eggs by the pubescence of the
host plant of S. parcesetosum. Vatanesever et al. (2003)
reported that cotton infested with B. tabaci constitutes
more suitable plant species for mass rearing due to short
development time, low mortality rate and high fecundity
of S. parcesetosum. In addition, B. tabaci is an insect that
is easily reared under laboratory conditions and suitable
for rearing S. parcesetosum (Yigit, 1992a). The data also
show that the interaction between S. parcesetosum and its
prey influences not only by prey species but also by the
suitability of the food plants used by the prey that serves
as food for the predator. In conclusion, S. parcesetosum
seems to prefer a number of whiteflies host plant species
for oviposition and can complete its full development
successfully on them.
et al., 2005). Serangium parcesetosum are common in
the Mediterranean region and both adults and larvae are
predaceous stages (Santos et al., 2009). Despite their
polyphagy, coccinellid adults tend to feed more on
certain types of food (Iperti, 1999) and the beneficial
effect that food has on individual predators leads to
increased rates of growth, development and fertility,
and decreased rates of mortality (Begon et al., 1996).
Moreover, larvae are the most voracious stages of
coccinellids requiring great amount of food to grow up
rapidly (Stathas, 2000). However, predation potential
data reveal that S. parcesetosum larvae and adults
exhibit the ability to prey voraciously upon many whitefly
species.
Predation potential of larval instars
The larvae of S. parcesetosum are able to prey
successfully upon different whitefly species reared on
different plants at different temperatures. The larvae
consume 310 and 261 of B. tabaci immatures/day at 25°C
and 23–33°C, respectively on cucumber (Al-Zyoud,
2008). Sengonca et al. (2005) mentioned a maximum
daily predation of 161 nymphs and 27 puparia at 18°C,
and 235 nymphs and 36 puparia of B. tabaci at 30°C on
cotton. Predation potential of the separate larval instars
of S. parcesetosum at 18°C indicated that L 1 instar
consumes a total of 115 nymphs or 27 puparia of B. tabaci.
The mean total predation increased with the progress
of development until it was the highest by the L4 instar
with 964 nymphs or 152 puparia. At 30°C, L1 instar fed
on 79 nymphs or 18 puparia, while L4 instar consumed
676 nymphs or 102 puparia of B. tabaci (Sengonca et al.,
2005). Asiimwe et al. (2007) reported that L1 instar
PREDATION POTENTIAL OF SERANGIUM
PARCESETOSUM
A successful biological control of a pest species
depends on the fact that the predator destroys, kills or
consumes a sufficient number of the pest to keep its
population bellow the economic threshold level (Sengonca
303
FIRAS AL-ZYOUD
consumed daily 99 nymphs and puparia of A. barodensis
and 170-200 eggs and immature stages of B. argentifolii
at 27°C (Patel et al., 1996), and 271 eggs or 23 puparia
of B. tabaci (Ahmad and Abboud, 2001).
consumed only 51 nymphs, while L4 feeds on 551 nymphs
of B. tabaci on cassava, indicating that L4 consumes 10fold higher than L 1 . The L 1 consumed a total of
44 nymphs or 18 puparia of T. vaporariorum, while
L4 instar consumed 722 nymphs or 110 puparia B. tabaci
(Al-Zyoud et al., 2005b). Means total of 122 and 75 (L1),
and 924 and 733 (L4) B. tabaci immatures were consumed
at 25°C and 23-33°C, respectively (Al-Zyoud, 2008).
Within 60 days of longevity, S. parcesetosum adults
consumed 2188 (males) and 1994 (females) nymphs or
727 (males) and 625 (females) puparia at 18°C, and
3948 (males) and 3577 (females) nymphs or 1601 (males)
and 1449 (females) puparia of B. tabaci at 30°C
(Sengonca et al., 2005), as well as 3842 (males) and
3507 (females) nymphs or 1482 (males) and 1368 (females)
puparia of T. vaporariorum (Al-Zyoud et al., 2005a).
While over 80 days of longevity, the predator consumed
7805 and 7502 of B. tabaci immatures at 25°C and
23–33°C, respectively (Al-Zyoud, 2008). The maximum
cumulative lifetime predation was measured at >10,000
of B. argentifolii consumed in the most long-lived
individuals (Legaspi et al., 1996). The daily predation
rate of adults increased with increasing temperature,
where it was 139, 181, and 187 of B. argentifolii immatures
at 20°C, 30°C and 40°C on cantaloupe, respectively
(Legaspi et al., 1996). In all the studies, females consumed
more prey than males, which justifies a stronger need
for nutrients for egg laying by females. Differences in
predation rate among the different studies could be
attributed to different prey species, prey stages, plant
species, temperatures and feeding periods used in the
different studies. It can be concluded that S. parcesetosum
successfully developed, survived, reproduced and fed
upon many whitefly species. Consequently, this ladybird
seems to have a potential to be a bio-agent of whiteflies,
which could be employed in biological control programs
against these pests under greenhouses and open field
conditions.
However, S. parcesetosum during its entire larval
development consumed more prey at 18°C (1566 nymphs
or 280 puparia) than at 30°C (1119 nymphs or 188
puparia) (Sengonca et al., 2005). This may be explained
by that the larval developmental period at 30°C was only
a half of that one at 18°C (Sengonca et al., 2004).
S. parcesetosum consumed 1012 nymphs or 184 puparia
of T. vaporariorum during its development (Al-Zyoud
et al., 2005b). The predatory larvae consumed more
B. tabaci at 25°C (1542) than at 23–33°C (1095
immatures) (Al-Zyoud, 2008). Timofeyeva and Nhuan
(1979) reported that S. parcesetosum larval instars
consumed a total of 900–1000 eggs of D. citri at 20–
23°C. In addition, S. parcesetosum consumed during its
larval duration 1678 eggs or 195 puparia of B. tabaci on
cabbage at 27°C (Ahmad and Abboud, 2001), 1055
nymphs of B. tabaci on cassava (Asiimwe et al., 2007),
and 671 nymphs and puparia of A. barodensis on
sugarcane at 27°C (Patel et al., 1996) respectively.
Differences in the results might be due to the fact that
different prey stages or species, host plants and
temperatures used in the different studies.
Predation potential of adults
The available data from prior studies on the predation
potential of S. parcesetosum adults indicated that predatory
females and males feed on 15 and 13 nymphs or 10 and
9 puparia of B. tabaci on the 1st day after adult emergence,
and reach a peak of 49 and 44 nymphs or 22 and 18
puparia/day at 18°C, respectively. While at 30°C, 41 and
23 nymphs or 24 and 23 puparia were consumed on the
1st day, and consumption reached a peak of 74 and 71
nymphs or 40 and 33 puparia/day by females and males,
respectively (Sengonca et al., 2005). S. parcesetosum
females and males fed on 31 and 30 nymphs or 20 and
18 puparia of T. vaporariorum on the 1st day after adult
emergence, and reached a peak of 84 and 71 nymphs or
34 and 29 puparia/day, respectively (Al-Zyoud et al.,
2005a). At 25 and 23-33°C, adults consumed 84 and
92 immatures of B. tabaci on the 1st day after adult
emergence and reached a peak of 144 and 130 immatures/
day, respectively (Al-Zyoud, 2008). S. parcesetosum adults
Predation potential by changing prey number
The prey’s population available in the agro-ecosystem
for a natural enemy will never be constant and fluctuates
in relation to many factors. To be considered as an efficient
natural enemy, a predator is expected to be able to adapt
itself to such a fluctuation in prey availability. However,
S. parcesetosum was smoothly able to adapt itself to
prey availability fluctuation. A range of 3–5, 6–9, 14–17
and 25–30 of B. tabaci puparia/day was consumed by
S. parcesetosum when 5, 10, 20 and 50 puparia were
offered/day, respectively (Sengonca et al., 2005). Thus,
daily predation rate became higher when more prey
was offered, in contrast, most of prey individuals offered
were consumed when the daily prey offer was only
5 puparia. These results are going along with a conclusion
made by Alvarado et al. (1997) who reported a considerable
increase in the daily predation rate in relation to prey
density.
304
Serangium parcesetosum: current status and future perspectives
Density-dependent response of Serangium parcesetosum
studies, S. parcesetosum has the ability to feed on all
developmental stages of whiteflies offered.
It is of vital importance in biological control to find
the predator response to prey because it may contribute
to stability of predator-prey system (Taylor, 1984). The
predator, S. parcesetosum imposes positive density
dependent with B. tabaci (type III functional response).
The functional response of S. parcesetosum can be
simulated by Hollings disc equation and expressed as
Ne=0.82N/1+0.0016N, and by the reciprocal linear
transformation of Hollings equation as y=1.2218x–0.0019.
The estimated search rate is 5.74 cm and the handling
time is 3 min (Araj et al., 2012). Predators having such
a type of response allow long-term population persistence
(Pech et al., 1992), and in turn will effectively stabilize
their prey population. S. parcesetosum causes higher
mortality levels at moderate whitefly densities. So, it is
recommended to use the predator at a moderate infestation
of whiteflies’.
Prey species preferences
Al-Zyoud and Sengonca (2004) offered five different
prey species to Serangium parcesetosum Sicard separately
on cotton, and it is found that predatory larvae and adults
have prey preference toward the whitefly species used
(B. tabaci and T. vaporariorum) consuming very few
individuals from the non-whitefly species Aphis gossypii,
Frankliniella occidentalis and Tetranychus urticae. In
addition, the predator had more preference for B. tabaci
rather than T. vaporariorum. In addition, when S. parcesetosum offered five different prey species together or
separately on cucumber, the predator also preferred the
whitefly species tested B. tabaci and T. ricini rather
than T. urticae, A. gossypii and Liriomyza huidobrensis
(Al-Zyoud, 2007). Legaspi et al. (1996) mentioned that
when S. parcesetosum was simultaneously offered the eggs
of Helicoverpa zea and Manduca sexta, and B. argentifolii
reared on poinsettia, cantaloupe and cucumber respectively,
the predatory adults did not feed on H. zea and M. sexta,
indicating a preference for B. argentifolii. Abboud and
Ahmad (1998) in a study conducted on the preference
of S. parcesetosum for different whitefly species
observed that the whitefly, Paraleyrodes minei
Laccarino is not suitable prey for S. parcesetosum,
while B. tabaci, D. citri and A. floccosus were found to
be suitable for the predator. In addition, they found
that S. parcesetosum prefers B. tabaci more than
D. citri and A. floccosus. Legaspi et al. (2001) noted that
S. parcesetosum is not as voracious on A. woglumi eggs
as on B. argentifolii nymphs. However, the degree of
preference of S. parcesetosum for one whitefly species
upon another might be due to size of the whitefly,
thickness and hardness of the cuticle, and many
other physical and chemical factors. Moreover, it might
be that nutrient differences among prey species have a
substantial impact on predator choice. Concomitantly,
S. parcesetosum is a specialist predator of whiteflies.
PREFERENCES OF SERANGIUM PARCESETOSUM
Before considering a predator in biological control, it
is important to investigate its affinity toward a certain
developmental stage of the target pest or even the pest
species to be controlled and a possible interaction with
other natural enemies. This is true especially when it is
taken into account that under greenhouses and open
field conditions there are naturally several pest species
that might serve as potential prey for the predator, in
addition, there are several natural enemies that could
interact with it.
Prey stage preferences
Investigating the preferred prey stage would be useful
in determining which developmental stage of the prey
is the most predated, and this will facilitate further
laboratory rearing of the predator, which is a prime
objective in biological control (Sahayaraj and Paulraj,
2001). However, S. parcesetosum L 2, L 4 instars and
adults prefer puparia and nymphs to the eggs of B. tabaci
on cotton (Al-Zyoud and Sengonca, 2004). Patel et al.
(1996) reported that the predator to be highly specific
and feeds voraciously on eggs, nymphs and puparia of
A. barodensis. S. parcesetosum predates eggs and
puparia of A. barodensis (Shah et al., 1986). According to
Ahmad and Abboud (2001), S. parcesetosum could
feed on all B. tabaci developmental stages. In general,
predation and preference depend mostly on the
characteristics of the prey’s tegument (Honda and Luck,
1995), relation between size of predator and prey, and
prey’s nutritional quality (Roger et al., 2000). However,
regardless of the whitefly species used in the different
Interaction and combined use of natural enemies
The predator, S. parcesetosum L2, L4, adult females
and males tend to avoid parasitized B. tabaci puparia by
En. formosa and feed instead on unparasitized ones. The
predator consumed daily 8.7 and 0.2 (L2), 11.1 and 0.6
(L4), 12.1 and 1.0 (male), and 10.5 and 0.2 (female)
unparasitized and parasitized B. tabaci puparia, respectively
(Al-Zyoud and Sengonca, 2004). In addition, larvae
and adults of S. parcesetosum significantly tend to avoid
parasitized puparia and feed instead on unparasitized
305
FIRAS AL-ZYOUD
puparia of B. tabaci by Er. mundus, i.e. 8.3 and 1.3 (L4)
and 8.5 and 1.3 (adult) unparasitized and parasitized
puparia, respectively (Al-Zyoud, 2007). Furthermore,
S. parcesetosum survivorship has not affected by the
rates of the entomopathogenic fungi, B. bassiana and
P. fumosoroseus, and cumulative predation showed that
S. parcesetosum sprayed with P. fumosoroseus consumes
prey at a rate similar to that in the control (Poprawski
et al., 1998). Overall, these results enhance the options
for the use of S. parcesetosum in pest management
programs in conjunction with parasitoids and pathogens.
The results suggest that because the parasitized whiteflies
by En. formosa and Er. mundus are currently in use
worldwide to control whiteflies (Abd-Rabou, 1999) from
one hand and on the other hand these parasitoids are
avoided by S. parcesetosum. There is a feasible potential
for integration of these natural enemies into whiteflies
management programs in order to provide a great level of
the pest suppression. In this regard, Zapata et al. (2003)
mentioned that release of Er. mundus in combination
with Macrolophus caliginosus provides a great level of
whitefly suppression.
Abboud (2001) mentioned that S. parcesetosum fed on
B. tabaci deposits its eggs singly or in irregular groups
on the plant leaves near the prey stages. It appears that
S. parcesetosum could lay its eggs singly or in groups.
Also, the results indicate that the presence of C. carnea
and plant species influence the distribution of eggs on
the leaves.
RELEASES OF SERANGIUM PARCESETOSUM
The predator, S. parcesetosum is a promising bioagent against many whitefly species because of its voracity
and preference. Both larvae and adults of S. parcesetosum
could feed on all developmental stages of whiteflies
(Kapadia and Puri, 1992; Ahmad and Abboud, 2001;
Al-Zyoud et al., 2005a.). However, because of the
success of S. parcesetosum in the laboratory and in order
to be considered as an efficient predator for a biological
control program and to be successfully used to control
whiteflies, it has been evaluated to check its effectiveness
in reducing the population of some whitefly species
under more natural conditions such as greenhouses and
open fields. However, when S. parcesetosum introduced
1 and 2 weeks after infestation with B. tabaci as well as
a control treatment on cotton plants under glasshouse
conditions, the number of B. tabaci was 75, 123 and
685 (1 predator: 25 whiteflies) in the last experimental
week (7th week), respectively (A-Zyoud et al., 2007).
On cucumber plants, the number of B. tabaci was
significantly higher in the control treatment compared with
1- and 2-week treatments when S. parcesetosum was
introduced at densities of 1:30 and 1:20. Initial whitefly
release rates (1:30 or 1:20) greatly affected the
final population density of the whitefly. This effect was
most evident when whitefly populations were left
uncontrolled, in which B. tabaci numbers in the last
experimental week were 955, 336 and 364 (1:30) as well
as 670, 253 and 267 (1:20) in control, 1 and 2 weeks after
S. parcesetosum introduction, respectively (Al-Zyoud,
2012). It could be concluded that release rate of 1 predator:
20 whiteflies would be more efficient in suppressing
the pest than 1:30. A single release of one adult
S. parcesetosum beetle was effective at stopping the
growth of B. tabaci populations on cucumber and
cotton for 7 weeks. In general, S. parcesetosum was able
to successfully feed, reproduce and consume B. tabaci
infested cotton and cucumber under greenhouse conditions.
In addition, the number of whitefly was lower when the
predator introduced one week rather than two weeks
after the whitefly infestation (A-Zyoud et al., 2007;
Al-Zyoud, 2012). In similar fashion, Ellis et al. (2001)
found that introduction of S. parcesetosum adults was
EGG LAYING BEHAVIOUR OF SERANGIUM
PARCESETOSUM
Studying of egg-laying behaviour and oviposition
strategy of a natural enemy is of a great value that leads
to a better understanding of its ecological characteristics
and helps positively in using it in a biological control
program against a pest species. A female insect must take
at least two decisions to oviposit on a host where to
lay its eggs and how many eggs to lay in each site. The
answers to these questions could explain the oviposition
strategy, which determines the insect fitness of
offspring and growth rate in the population (Danho
and Haubruge, 2003). However, Al-Zyoud et al. (2005b)
investigated the egg-laying behaviour of S. parcesetosum
in the absence and presence of C. carnea, one of the
main predators associated with B. tabaci population, on
cucumber and cotton infested with B. tabaci. They found
that S. parcesetosum prefers to lay its eggs between the
veins and close to the veins in the absence of C. carnea,
while in its presence more eggs were deposited close to
veins and petiole on cucumber leaves. In contract, on
cotton leaves S. parcesetosum prefers to deposit its
eggs close to the veins and petiole in the absence and
presence of C. carnea. Timofeyeva and Nhuan (1979)
stated that S. parcesetosum fed on D. citri lays its eggs
on the under surface of citrus leaves. S. parcesetosum
deposits its eggs singly on the under surface of eggplant
leaves infested with B. tabaci (Kapadia and Puri, 1992).
According to Patel et al. (1996), S. parcesetosum fed on
A. barodensis lays its eggs singly. While, Ahmad and
306
Serangium parcesetosum: current status and future perspectives
infecting a greenhouse crop of poinsettias. Whitefly
densities within the control treatments were considerably
greater than those of each of the two natural enemy
treatments. At the end of the study (week 13), the whitefly
population was less than 1/100 and 1/150 in the greenhouse
area receiving both natural enemies and S. parcesetosum
alone, respectively from those in the control (Weaver
and Ciomperlik, 2000a). Furthermore, releases of
S. parcesetosum were evaluated for their ability to
disperse throughout a greenhouse crop of poinsettias
infested with B. argentifolii. Whiteflies were introduced
at a rate of 1.25 adult/plant in week 0 into two separate
greenhouses and releases of S. parcesetosum were made
on weeks 5, 7, and 9. However, results indicated that if
whitefly densities were high, the beetles did not disperse
as readily as when whitefly densities were low (Weaver
and Ciomperlik, 2000b). Heinz and Parrella (1994b)
recovered several adult D. catalinae three weeks after
the last release, but no evidence of successful predator
reproduction was reported. In contrast, S. parcesetosum
larvae were first observed 1 week after adults have
been released (A-Zyoud et al., 2007 Al-Zyoud, 2012).
However, S. parcesetosum would be useful especially
for suppressing localized pest population in the
greenhouse. An additional positive feature of
S. parcesetosum that its ability to distinguish between
parasitized and unparasitized B. tabaci by En. formosa
(Al-Zyoud and Sengonca, 2004) and Er. mundus (AlZyoud, 2007) and feed on more unparasitized whiteflies.
In Jordan, Sharaf and Hassan (2003) mentioned a high
parasitization rate when either Er. mundus (72.2%) or
En. formosa (75.8%) were released against B. tabaci at
a ratio of 1 parasitoid: 2 whiteflies. As an obligate whitefly
predator with a voracious feeding potential, S. parcesetosum is capable for checking rapid increases in
whitefly populations, thus potentially enabling whitefly
parasitoid species such as Eretmocerus or Encarsia to
suppress whiteflies to acceptable thresholds. Thus, there
is a feasible potential for integration of the predator and
the two parasitoids into a biological control program to
suppress B. tabaci. This conclusion is supported by
Heinz and Nelson (1996) who found that the specific
whitefly predator, D. catalinae provided the greatest
suppression of the silverleaf whitefly when used in
conjunction with Encarsia. Also, Zapata et al. (2003)
showed that releases of Er. mundus alone or in combination
with M. caliginosus provided a great level of whitefly
suppression. Based on these data it appears that
S. parcesetosum might be best suited for inclusion in a
multiple species biological control approach for management
of whiteflies. Another positive feature which makes the
predator, S. parcesetosum more distinguished and effective
extremely effective at stopping the growth of B. argentifolii
population on poinsettias under greenhouse conditions
for 10 weeks. They further mentioned that after six
weeks of introducing S. parcesetosum, B. argentifolii
population densities were dramatically lower in the
cages with S. parcesetosum than in the control cages. An
early introduction of S. parcesetosum, while the density
of B. tabaci population is still low, would be more effective
in its control. On eggplants infested by B. tabaci, followed
by the introduction of S. parcesetosum within three
weeks at weekly intervals at rates of 0, 3, 6 adults/plant,
the number of whiteflies increased in treated cages
until the 3rd week, and then began to decrease 7 weeks
later. Whereas, the density of whitefly population in
the control treatment increased 3-fold during the same
period (Abboud et al., 2006).
Reductions in B. tabaci population of 65 and 62%
(1:30) as well as 62 and 60% (1:20) on cucumber plants,
and 89 and 82% (1:25) on cotton plants were reported
in the last experimental week (7th week) when the predator
was introduced 1 and 2 weeks, respectively (A-Zyoud
et al., 2007; Al-Zyoud, 2012). B. tabaci population in
cages receiving 2 and 4 S. parcesetosum adults/plant
showed 56 and 53% reductions on eggplants, respectively
(Kutuk et al., 2008). In addition, when 1 S. parcesetosum
was released in cages filled with A. woglumi eggs on
grapefruit, it was found that predation by S. parcesetosum
for 12 days reduced egg hatch by 12.5% (Legaspi et al.,
2001). Variation among the different studies might be
due to differences in prey species or strain, temperature,
host plant and release rate used in the different studies.
However, it is to be mentioned that even without a
reproductive success, introducing S. parcesetosum prevents
B. tabaci population from increasing over a 7-weekperiod (Al-Zyoud et al., 2007 Al-Zyoud, 2012) and B.
argentifolii population over a 10-week-period (Ellis
et al., 2001). This can be explained by the fact that
laboratory studies up to date show that the ladybird’s
adults could survive for 2-6 months (Sengonca et al., 2004)
and 3 months (Legaspi et al., 1996 Al-Zyoud et al., 2007).
In addition, the predator’s adults are voracious feeders
capable for consuming large numbers of whiteflies,
where they reached just over 80 days of longevity to 7805
whiteflies (Al-Zyoud, 2008), and >10,000 B. argentifolii/
lifetime (Legaspi et al., 1996). Therefore, depending on
these results, it appears that this success in controlling
whiteflies was primarily, in addition to the feeding of
the larvae, due to the prolonged survival and continuous
feeding of S. parcesetosum adults.
Furthermore, En. formosa and S. parcesetosum were
released at a rate of 1 adult/plant to control B. argentifolii
307
FIRAS AL-ZYOUD
population persistence, and in turn will effectively
stabilize its prey population. In addition, S. parcesetosum
could feed on all developmental stages of whiteflies
offered, and has a prey preference toward whitefly
species used rather than the non-whitefly species. Thus,
S. parcesetosum is a specialist predator of whiteflies.
Furthermore, S. parcesetosum tended to avoid parasitized
puparia of B. tabaci by En. formosa and Er. mundus
and feed instead on unparasitized puparia. Moreover,
S. parcesetosum sprayed with P. fumosoroseus consumed
prey at a rate similar to that of the control. Thus, there
is a feasible potential for integration of these natural
enemies into management programs for whiteflies in order
to provide a great level of suppression.
compared to other predators is that the predator is
specific for whiteflies (Legaspi et al., 1996 Abboud
and Ahmad, 1998; Al-Zyoud and Sengonca, 2004;
Al-Zyoud, 2007).
Releases of S. parcesetosum in citrus orchards
infested with Diaphernia citri resulted in its establishment
on citrus and dispersal throughout the citrus-growing
regions in Turkey. Also, S. parcesetosum could tolerate
large temperature intervals in the region of Turkey. The
success in colonization of S. parcesetosum within a
certain period shows its high potential of searching
capacity in addition to prey suitability (Yigit and Canhalal,
2005). Antadze and Timofeyeva (1975) indicated that
S. parcesetosum could overwinter in Georgia where
the temperature was –2°C. While, Yasnosh and Chaidze
(1986) mentioned that the predator overwintered as
adults and could resist –6°C to –8°C. On cotton, the
predator population increased in the 1st generation to
9-fold, and in cages into which 16-18 adult coccinellids
were introduced, produced an average of 157 adults (Yigit,
1992a).
Under greenhouse conditions, B. tabaci population
was significantly lower when S. parcesetosum was
introduced after 1 or 2 weeks than control treatment. Also,
the number of B. tabaci was lower when the predator
was introduced after 1 week rather than 2 weeks. A single
release of one S. parcesetosum/plant was effectively
checked further increases in prey population on
cotton and cucumber for up to 7 weeks, and on poinsettias
for 10 weeks. It is speculated that early release of
S. parcesetosum would be more effective in biological
control of whiteflies. S. parcesetosum could spread
out throughout cotton orchards with heavily infested
by D. citri by forming a colony, and tolerate large
temperature intervals. It is concluded that releases of
the predatory beetle should preferably be done in central
point in an orchard, heavily infested by the prey to spread
the predator to other orchards.
CONCLUSION
The ladybird, S. parcesetosum is a specialist, oligophagous and efficient predator that has demonstrated a
potential for biological control of many whiteflies.
S. parcesetosum is able to develop successfully on many
whitefly species and it could survive for up to 6 months.
S. parcesetosum adults survived for a period of time
on artificial nutritional sources, which may have an
advantage in stabilizing its population dynamics. An
artificial growth medium was successfully used to rear
S. parcesetosum for 3 generations.
Long survival of S. parcesetosum adults accomplished
by their voracious feeding is a great feature that resulted
in a successful control of whiteflies. These information
will lead to enhance the options for using this specialized
whitefly predator in pest management programs to control
many whitefly species in greenhouses and open fields.
Finally, the ladybird predator, S. parcesetosum showed
the ability to develop, survive, reproduce and prey
successfully upon and build up its population as well
as cause a high reduction in whiteflies population.
Consequently, it is likely that S. parcesetosum could
function effectively as the sole biological control agent or
in conjunction with other natural enemies to provide a
great level of whiteflies suppression, as well as to develop
new managing strategies to successfully suppress these
worldwide pests. However, additional studies mentioned
below are worth consideration: (1) searching behavior of
S. parcesetosum that permits subsistence at low whitefly
densities; (2) optimal exploitation of S. parcesetosum
must consider the fact that several species may be present
Cotton infested with B. tabaci constituted more
suitable plant species for mass rearing of S. parcesetosum.
S. parcesetosum seems to occupy a number of host
plant species for oviposition and can complete its
development successfully on them. Data presented herein
provide opportunities to better understand interactions of
the plant-whitefly-predator and demonstrated that
successful biological control of pests should integrate the
environmental aspects of each trophic level.
The predator exhibited the ability to prey successfully
upon many whitefly species. The predatory larvae could
consume up to 1566 whitefly immatures/day during its
entire larval development and adults feed on >10,000
B. argentifolii in the most long-lived individuals. In
addition, S. parcesetosum imposes positive density
dependent with B. tabaci, which allows long-term
308
Serangium parcesetosum: current status and future perspectives
contemporaneously and act in a complementary way;
(3) the effect of insecticides on S. parcesetosum; (4) the
discontinuous nature of annual crops which do not
provide a stable environment for the predator establishment
and finally, (5) the presence of other pests that may require
additional management considerations.
and its interaction with another natural enemy.
Pakistan J Biol Sci. 10: 2159–2165.
Al-Zyoud F. 2008. Biology and predation potential of
the Indian ladybird Serangium parcesetosum on
Bemisia tabaci. Jordan J Agric Sci. 4: 26–40.
Al-Zyoud F. 2012. Greenhouse cage evaluation of
Serangium parcesetosum Sicard (Col.: Coccinellidae)
as predator of the cotton whitefly Bemisia tabaci
(Genn.) (Hom.: Aleyrodidae). Jordan J Agric Sci. (In
print).
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